Differential ripple propagation along the hippocampal longitudinal axis
Abstract
Hippocampal ripples are highly synchronous neural events critical for memory consolidation and retrieval. A minority of strong ripples has been shown to be of particular importance in situations of increased memory demands. The propagation dynamics of strong ripples inside the hippocampal formation are, however, still opaque. We analyzed ripple propagation within the hippocampal formation in a large open access dataset comprising 267 Neuropixel recordings in 49 awake, head-fixed mice. Surprisingly, strong ripples (top 10% in ripple strength) propagate differentially depending on their generation point along the hippocampal longitudinal axis. The septal hippocampal pole is able to generate longer ripples that engage more neurons and elicit spiking activity for an extended time even at considerable distances. Accordingly, a substantial portion of the variance in strong ripple duration (R² = 0.463) is explained by the ripple generation location on the longitudinal axis, in agreement with a possible distinctive role of the hippocampal septal pole in conditions of high memory demand. Moreover, we observed that the location of the ripple generation has a significant impact on the spiking rate modulation of different hippocampal subfields, even before the onset of the ripple. This finding suggests that ripple generation location plays a crucial role in shaping the neural activity across the hippocampus.
Data availability
All the code used to process the dataset is available at https://github.com/RobertoDF/De-Filippo-et-al-2022, pre-computed data structures can be downloaded at 10.6084/m9.figshare.20209913. All figures and text can be reproduced using code present in this repository, each number present in the text is directly linked to a python data structure. The original dataset is provided by the Allen Institute and available at https://allensdk.readthedocs.io/en/latest/visual_coding_neuropixels.html.
-
Visual Coding - Neuropixelshttps://knowledge.brain-map.org/data/4YYLRZZGK82FQ85NIH8/summary.
Article and author information
Author details
Funding
Deutsche Forschungsgemeinschaft (184695641 - SFB 958)
- Dietmar Schmitz
Deutsche Forschungsgemeinschaft (327654276 - SFB 1315)
- Dietmar Schmitz
European Research Council (810580)
- Roberto de Filippo
NeuroCure Exzellenzcluster (Exc-2049-390688087)
- Dietmar Schmitz
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2023, de Filippo & Schmitz
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 1,514
- views
-
- 221
- downloads
-
- 10
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Neuroscience
Evidence accumulation models (EAMs) are the dominant framework for modeling response time (RT) data from speeded decision-making tasks. While providing a good quantitative description of RT data in terms of abstract perceptual representations, EAMs do not explain how the visual system extracts these representations in the first place. To address this limitation, we introduce the visual accumulator model (VAM), in which convolutional neural network models of visual processing and traditional EAMs are jointly fitted to trial-level RTs and raw (pixel-space) visual stimuli from individual subjects in a unified Bayesian framework. Models fitted to large-scale cognitive training data from a stylized flanker task captured individual differences in congruency effects, RTs, and accuracy. We find evidence that the selection of task-relevant information occurs through the orthogonalization of relevant and irrelevant representations, demonstrating how our framework can be used to relate visual representations to behavioral outputs. Together, our work provides a probabilistic framework for both constraining neural network models of vision with behavioral data and studying how the visual system extracts representations that guide decisions.
-
- Neuroscience
How and why is working memory (WM) capacity limited? Traditional cognitive accounts focus either on limitations on the number or items that can be stored (slots models), or loss of precision with increasing load (resource models). Here, we show that a neural network model of prefrontal cortex and basal ganglia can learn to reuse the same prefrontal populations to store multiple items, leading to resource-like constraints within a slot-like system, and inducing a trade-off between quantity and precision of information. Such ‘chunking’ strategies are adapted as a function of reinforcement learning and WM task demands, mimicking human performance and normative models. Moreover, adaptive performance requires a dynamic range of dopaminergic signals to adjust striatal gating policies, providing a new interpretation of WM difficulties in patient populations such as Parkinson’s disease, ADHD, and schizophrenia. These simulations also suggest a computational rather than anatomical limit to WM capacity.